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. 2024 Nov 1;16(11):evae232.
doi: 10.1093/gbe/evae232.

Aberrant Mitochondrial tRNA Genes Appear Frequently in Animal Evolution

Iuliia Ozerova  1 , Jörg Fallmann  1   2 , Mario Mörl  3 , Matthias Bernt  4 , Sonja J Prohaska  5   6 , Peter F Stadler  1   7   8   9
Affiliations

Aberrant Mitochondrial tRNA Genes Appear Frequently in Animal Evolution

Iuliia Ozerova et al. Genome Biol Evol. .

Abstract

Mitochondrial tRNAs have acquired a diverse portfolio of aberrant structures throughout metazoan evolution. With the availability of more than 12,500 mitogenome sequences, it is essential to compile a comprehensive overview of the pattern changes with regard to mitochondrial tRNA repertoire and structural variations. This, of course, requires reanalysis of the sequence data of more than 250,000 mitochondrial tRNAs with a uniform workflow. Here, we report our results on the complete reannotation of all mitogenomes available in the RefSeq database by September 2022 using mitos2. Based on the individual cases of mitochondrial tRNA variants reported throughout the literature, our data pinpoint the respective hotspots of change, i.e. Acanthocephala (Lophotrochozoa), Nematoda, Acariformes, and Araneae (Arthropoda). Less dramatic deviations of mitochondrial tRNAs from the norm are observed throughout many other clades. Loss of arms in animal mitochondrial tRNA clearly is a phenomenon that occurred independently many times, not limited to a small number of specific clades. The summary data here provide a starting point for systematic investigations into the detailed evolutionary processes of structural reduction and loss of mitochondrial tRNAs as well as a resource for further improvements of annotation workflows for mitochondrial tRNA annotation.

Keywords: armless tRNAs; mitochondrial tRNAs; tRNA annotation; tRNA loss; tRNA secondary structure; truncated tRNAs.

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Figures

Fig. 1.
Fig. 1.
Length distribution of mt-tRNA genes predicted by mitos2 for the annotated mitogenomes. Overall, the overwhelming majority has a length around 70, corresponding to the canonical cloverleaf structure (shown in blue). Aberrant mt-tRNAs (orange) are typically shorter. Outliers are most likely incorrect predictions.
Fig. 2.
Fig. 2.
Distribution of mt-tRNA shapes in Metazoa. Manually curated data from mitos2 annotation grouped according to the NCBI taxonomy (leaves are collapsed at the family level). The average number of cloverleaf (blue) and truncated (orange) mt-tRNAs per genome is shown. Duplicated tRNA genes are ignored. In cases where the number of mt-tRNA families is less than the metazoan consensus of 22, the plot shows a white indentation. The inset in the center shows a histogram of relative abundances of structurally aberrant tRNAs. mt-tRNA-X was excluded from the analysis. A version with full annotation can be found in supplementary file S2, Supplementary Material online. Note that the NCBI Taxonomy places Acanthocephala within Lophotrochozoa and not within Gnathifera (Vasilikopoulos et al. 2024).
Fig. 3.
Fig. 3.
Distribution of mt-tRNA shapes in Cnidaria: widespread mt-tRNA loss. Overview of mt-tRNA shapes curated from the mitos2 pipeline annotation. The presence of an mt-tRNA for a given anticodon/amino acid with color indicates the shape. The color indication is the following: canonical cloverleaf shapes (blue), the loss of one arm (orange), and the loss of both arms (red); mt-tRNA losses are shown in white. Black entries denote two tRNAs with mixed annotations coming from different shapes for the same isoacceptor class in the same species. mt-tRNA-X denotes predictions with an anticodon that is a stop codon in the standard genetic code. Version with full annotation can be found in supplementary file S3, Supplementary Material online.
Fig. 4.
Fig. 4.
Distribution of mt-tRNA shapes in Lophotrochozoa. Overview of mt-tRNA shapes curated from the mitos2 pipeline annotation. The presence of an mt-tRNA for a given anticodon/amino acid with color indicates the shape. The color indication is the following: canonical cloverleaf shapes (blue), the loss of one arm (orange), and the loss of both arms (red); mt-tRNA losses are shown in white. Black entries denote two tRNAs with mixed annotations coming from different shapes for the same isoacceptor class in the same species. mt-tRNA-X denotes predictions with an anticodon that is a stop codon in the standard genetic code. Version with full annotation can be found in supplementary file S4, Supplementary Material online.
Fig. 5.
Fig. 5.
Distribution of mt-tRNA shapes in Nematoda. Overview of mt-tRNA shapes curated from the mitos2 pipeline annotation. The presence of an mt-tRNA for a given anticodon/amino acid with color indicates the shape. The color indication is the following: canonical cloverleaf shapes (blue), the loss of one arm (orange), and the loss of both arms (red); mt-tRNA losses are shown in white. Black entries denote two tRNAs with mixed annotations coming from different shapes for the same isoacceptor class in the same species. mt-tRNA-X denotes predictions with an anticodon that is a stop codon in the standard genetic code. Version with full annotation can be found in supplementary file S5, Supplementary Material online.
Fig. 6.
Fig. 6.
Distribution of mt-tRNA shapes in Arachnida. Overview of mt-tRNA shapes curated from the mitos2 pipeline annotation. The presence of an mt-tRNA for a given anticodon/amino acid with color indicates the shape. The color indication is the following: canonical cloverleaf shapes (blue), the loss of one arm (orange), and the loss of both arms (red); mt-tRNA losses are shown in white. Black entries denote two tRNAs with mixed annotations coming from different shapes for the same isoacceptor class in the same species. mt-tRNA-X denotes predictions with an anticodon that is a stop codon in the standard genetic code. Version with full annotation can be found in supplementary file S6, Supplementary Material online.
Fig. 7.
Fig. 7.
Romanomermis genus: mt-tRNA shapes obtained from different sources. mt-tRNA shapes were collected from mitos2 pipeline, shortened CM set (custom CMs) with further locus-specific filtration and CM set, constructed with published Enoplea alignment (Jühling et al. 2012b). All candidates were manually checked, and the final distinction between D- and T-armless mt-tRNA is presented.
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